Effect of temperature on functional response of Aphidius gifuensis (: ) parasitizingMyzus persicae (Hemiptera: Aphididae) Muhammad Akbar Zafar Khan, Qifu Liang, Munoz San Martin Maria, and Tong-Xian Liu*

Abstract Aphidius gifuensis Ashmead (Hymenoptera: Braconidae) is a common parasitoid of aphids including the green peach aphid, Myzus persicae (Sulzer) (He- miptera: Aphididae). To maximize the use of A. gifuensis for biological control of M. persicae, the functional response ofA. gifuensis using M. persicae as a host was determined at 4 constant temperatures (15, 20, 25, and 30 °C) and 20 host densities (5, 10, 15, increased incrementally by 5, to a maximum of 100) on a 6-leaf sweet pepper plant (30 cm in height) over a 24 h period. Roger’s random parasitoid equation (RRPE) and Holling’s disc equation (HDE) were used to fit the data. The results showed that functional responses at all temperatures were type II, and the instantaneous attack rate (a) in both models increased as temperature increased from 15 to 25 °C and then decreased at 30 °C. The highest instantaneous attack rate (a) for A. gifuensis was −1 −1 at 25 °C for the 2 models, 1.3203 ± 0.0415 d for HDE and 4.295e+03 d for RRPE. The handling time (Th) for A. gifuensis by HDE was between 0.0105 ± 0.0002 d at 20 °C and 0.0214 ± 0.0009 d at 30 °C and by RRPE was between 1.265e−02 ± 3.808e−04 d at 20 °C and 0.0218 ± 0.0010 d at 30 °C. Aphidius gifuensis achieved its highest parasitism rate at medium temperatures. The results from this study showed that A. gifuensis performed best at 20 °C, suggesting that this parasitoid will be more effective as a biological control agent for M. persicae when the temperature is under 30 °C.

Key Words: biological control; Holling’s disc model; Roger’s random parasitoid model; sweet pepper; China

Resumen Aphidius gifuensis Ashmead (Hymenoptera: Braconidae) es uno de los parásitos comunes de áfidos, entre los que se incluye el áfido verde del melo- cotón, Myzus persicae (Sulzer) (Hemiptera: Aphididae). Para potenciar el uso de A. gifuensis como control biológico de M. persicae, se determinó la respuesta funcional de A. gifuensis utilizando M. persicae como hospedador a cuatro temperaturas constantes (15, 20, 25 y 30 °C) y 20 densidades de hospedador (5, 10, 15, aumentó gradualmente por 5, a un máximo de 100) en una planta de pimiento dulce de 6 hojas (30 cm de altura) durante un periodo de 24 horas. Se utilizaron el modelo de parásito aleatorio de Roger y el modelo de disco de Holling para ajustar los datos. Los resultados mostraron que las respuestas funcionales en todas las temperaturas fueron de tipo II y los resultados mostraron que la tasa de ataque instantáneo (a) en ambos modelos incrementó a medida que la temperatura incrementaba desde 15 a 25 °C y después disminuyó a 30 °C. La tasa más alta de ataque instantáneo para A. gifuensis se obtuvo a 25 °C en ambos modelos, 1.3203 ± 0.0415 día−1 por el modelo de disco de Holling y 4.295e+03 día−1 por el

modelo de Roger. El tiempo de manipulación (Th) para A. gifuensis por el modelo de Holling fue entre 0.0105 ± 0.0002 día a 20 °C y 0.0214 ± 0.0009 día a 30 °C y por el modelo de Roger fue entre 1.265e−02 ± 3.808e−04 día a 20 °C y 0.0218 ± 0.0010 día a 30 °C. Aphidius gifuensis logró la tasa de parasitismo más alta a temperaturas medias. Los resultados de este estudio mostraron que A. gifuensis actuó mejor a 20 °C, lo que sugiere que este parásito puede ser más efectivo como control biológico de M. persicae cuando la temperatura es inferior a 30 °C.

Palabras Clave: control biológico; modelo de disco de Holling; parasitoide modelo al azar de Roger; pimienta dulce; China

Insect parasitoids are very important in population and behavioral tion of eggs or handling time problems in the case of parasitoids (Getz studies because they are abundant in nature and are significant bio- & Mills 1996). The type of functional response depends upon the re- logical control agents of many pests (Godfray 1994). The objective of sponse curve’s shape below the upper limit. Response curves show the ecological studies on parasitoids is to find the properties that are es- parasitoid–host interaction and are helpful in forecasting suitability of sential for the parasitoid to be a good biocontrol agent. Among these parasitoids in biological control programs. properties is their functional response (Berryman 1999). The function- Generally, the functional response is the intake rate by the consumer al response describes the number of hosts attacked by an individual as a function of food density. There are 3 types, known as Holling’s type I, natural enemy in relation to host density over a given time period (Sol- II, and III. The type I response shows a linear increase, the type II response omon 1949). The number of hosts attacked increases as host densities shows a hyperbolic increase, and the type III response shows a sigmoidal increase, and there is an upper limit to the number of hosts attacked, increase in the number of hosts attacked (Holling 1959). The parasitoid– due to satiation in the case of predators (Mills 1982), and due to limita- host population is altered by each type of functional response. In the type

State Key Laboratory of Crop Stress Biology for Arid Areas, Northwest A&F University, Yangling, Shaanxi 712100, China; and Key Laboratory of Northwest Loess Plateau Crop Pest Management of Ministry of Agriculture, Northwest A&F University, Yangling, Shaanxi 712100, China; E-mail: [email protected] (M. A. Z. K.), [email protected] (Q. L.), [email protected] (M. S. M. M.), [email protected] (T.-X. L.) *Corresponding author; E-mail: [email protected] (T.-X. L.)

696 2016 — Florida Entomologist — Volume 99, No. 4 Khan et al.: Functional response of Aphidius gifuensis on Myzus persicae 697 I functional response, there is density-independent parasitism; in type II, miculite, peat moss, and perlite “Pindstrup Substrate” (Pindstrup Hor- there is inverse density-dependent parasitism; and in type III, there is a ticulture Ltd., Shanghai, China) at a 4:1:1 ratio by volume. The sweet direct density-dependent interaction at low host density that leads to the pepper plants in plastic pots were placed in growth chambers. One stabilization of parasitoid–host interaction. As the host density increases, plant was grown per plastic pot. Plants were germinated in growth the response also increases and then levels off (Hassell 2000). Stability is a chambers maintained at 25 ± 1 °C, 75 ± 5% RH, with a light intensity of very important aspect of biological control programs. 1,400 to 1,725 lx and a photoperiod of 16:8 h L:D. After germination, Aphidius gifuensis Ashmead (Hymenoptera: Braconidae) is a very sweet pepper plants were transferred to air-conditioned insectaries at important parasitoid of Myzus persicae (Sulzer) (Hemiptera: Aphididae) 25 ± 1 °C, 65 ± 5% RH, with a light intensity of 1,400 to 1,725 lx and in Japan (Takada 2002) and China (Pan & Liu 2014). Aphidius species are a photoperiod of 16:8 h L:D. Sweet pepper plants at the 6-leaf stage well-known parasitoids and are extensively used in biological control were used for functional response experiments. Dry soluble fertilizer programs of aphids (Starý et al. 1988). The genus Aphidius comprises “Harvest More 20-20-20+TE” (Stoller Enterprises, Inc, Houston, Texas) many species including Aphidius colemani Viereck, Aphidius ervi Haliday, at a rate of 1 g/L of water was applied to plants at 7 d intervals. and Aphidius matricariae Haliday. These species are commercially avail- able and are mostly used in greenhouses and fields against aphids (van Steenis & El-Khawass 1995; Grasswitz 1998). Aphidius are small wasps CULTURE whose females lay eggs in aphid nymphs, and the larvae of the wasps Myzus persicae living aphids and mummies were collected from consume the aphids from inside. As the larvae mature and the aphids sweet pepper in greenhouses at Yangling City, Shaanxi Province, China, in are killed, the aphids turn into mummies, and after pupation adult wasps Jun 2013. Aphids were reared on sweet pepper plants in large net cages emerge from the mummies (Hagvar & Hofsvang 1991). Evaluation of the (60 × 60 × 60 cm) in air-conditioned insectaries at 25 ± 2 °C, 65 ± 5% RH, parasitism potential of these parasitoids is very important in developing with light intensity of 1,400 to 1,725 lx and a photoperiod of 16:8 h L:D. integrated pest management programs for aphid control. After emergence from mummies, the parasitoids were reared on sweet The green peach aphid, M. persicae, is a common pest of veg- pepper plants infested with M. persicae. The populations of aphids and etable crops belonging to the families Solanaceae and Brassicaceae. parasitoids were maintained in air-conditioned insectaries for many gen- The distribution of M. persicae is throughout the southern to the erations and then used in functional response experiments. northern temperate zones. Myzus persicae has more than 875 sec- ondary host plant species which include vegetables, crops, and orna- mental plants (Ro et al. 1998). Aphids damage plants in many ways; FUNCIONAL RESPONSE STUDY by direct feeding, by releasing honeydew, or by transmitting viruses, There were 4 temperatures (15, 20, 25, and 30 °C), 20 aphid densi- for example, Cucumber mosaic virus, Pepper veinal mottle virus, and ties (from 5 to 100 per plant, at increments of 5), and 4 replications Sweet potato leaf curl virus (Schepers 1988). Chemical control has of all treatments. Individual pots, containing 1 sweet pepper plant at commonly been used against aphids in greenhouses (Parrella et al. the 6-leaf stage were covered by a plastic cage (30 × 15 cm). The top 1999), but at present there is an increase in insecticide resistance and of the cage was covered by a nylon net for air transfer. A small Petri cross-resistance in M. persicae, and insecticides also cause environ- dish (3.5 × 1 cm) with 10% honey water solution was placed inside mental pollution (Lee & Kang 2004). To reduce insecticide use, natu- the plastic cage for the parasitoids. These cages were placed in growth ral enemies of aphids are being used for biological control to protect chambers. Myzus persicae 3rd instars were used in this study. After greenhouse crops. In greenhouse crops, the objective is to suppress emergence from mummies, A. gifuensis wasps were sexed, and 1 male the pest population in the latent phase of pest development rather and 1 female were allowed to mate in small vials; 1 to 2 d later, 1 mated than to reduce an already dense pest population. The early introduc- female was released in each plastic cage for each aphid density for 24 tion of a natural enemy in order to decrease latent phase growth is h and then removed. Aphids were observed daily for the presence of aimed to cause mortality associated with a functional response (Wie- brownish mummies. denmann & Smith 1997). In many previous studies scientists have used Petri dishes for func- tional response experiments, but in this study we used sweet pepper DATA ANALYSES plants (6-leaf stage) in plastic pots for functional response experi- A 2-step approach was used to analyze the experimental data for ments. The objective of this study was to determine the effect of tem- functional responses. Data were first checked to see whether they peratures on the functional response curve. We tested 2 functional showed a type II or type III functional response. A cubic logistic regres- response curves to determine which model fits best. These models will sion (Equation 1) between the proportion of aphids parasitized and provide information that can be used in developing better pest man- the number of aphids was performed to find the shape of the curve agement programs against aphids in greenhouses and fields. (Juliano 2001). N exp(P + P N + P N2 + P N3) par = 0 1 2 3 (1) N 1 + exp(P + P N + P N2 + P N3) Materials and Methods 0 1 2 3

Experimental work was done in the Key Laboratory of Applied Ento- mology, Northwest A&F University, Yangling (34.2833°N, 108.0617°E), Npar is the number of aphids parasitized, N is the number of aphids

Shaanxi, China. The experiments were started on 1 Jan 2014 and ended offered, andP o, P1, P2 and P3 are the intercept, linear, quadratic, and cu- on 30 Dec 2015. bic coefficients, respectively. If the linear coefficient (P1) is significantly negative, the response is type II, and if it is significantly positive, the response is type III (Juliano 2001). HDE and RRPE were used to calcu- HOST PLANT late the handling times and attack coefficients of a type II functional Sweet pepper seeds, Capsicum annum L. ‘Qiemen-Tianjiao’ (So- response. Equation 2 expresses HDE (Holling 1959), and Equation 3 lanaceae), were grown in plastic pots (15 × 15 cm) a mixture of ver- expresses RRPE (Rogers 1972). 698 2016 — Florida Entomologist — Volume 99, No. 4 Attack rates (a) of A. gifuensis modeled by HDE are presented in aTN −1 (2) Table 2. At 25 °C, the attack rate was 1.3203 ± 0.0415 d and was sig- Npar = 1 + aThN nificantly greater than at the others temperatures. At 20 °C, the attack rate was 1.3142 ± 0.0312 d−1 and was significantly lower than at 25 °C. At 15 °C, the attack rate was 1.1323 ± 0.0191 −1d and was significantly aT N = N 1 – exp – (3) lower than at 20 °C. At 30 °C, the attack rate was 0.7999 ± 0.0393 d−1 par  1 + aT N   h  and was significantly lower than at all other temperatures. Attack rates were highest at 20 and 25 °C, indicating that parasitism was greatest N is the number of aphids parasitized, N is the number of aphids par at these temperatures. offered,a is attack rate,T is handling time, andT is the total time offered h Handling times (T ) of A. gifuensis modeled by HDE are also pre- for parasitoid. R version 2.15.0 (R Development Core Team 2012) statisti- h cal software was used for parameter estimation in all above equations. sented in Table 2. At 30 °C, the handling time was 0.0214 ± 0.0009 d If R statistical software was unable to give results, we used Solver tool in and was significantly longer than at all other temperatures. At 15 and Microsoft Excel 2010 for parameter estimation in nonlinear regression. 25 °C, handling times were the same with 0.0120 ± 0.0003 d and were shorter than at 30 °C. At 20 °C, the handling time was 0.0105 ± 0.0002 d and was the shortest among all the temperatures, indicating that Results parasitism was best at 20 °C. Thus, according to HDE, the attack rate was highest at 20 and 25 Logistic regressions for A. gifuensis at all 4 temperatures showed °C and the handling time shortest at 20 °C. Equations 8, 9, 10, and 11 significant linear parameters P1 < 0 (Table 1). The number of aphids show HDE with modeled values of attack rate (a) and handling time (Th) parasitized byA. gifuensis hyperbolically approached the asymptote as at 15, 20, 25, and 30 °C, respectively. aphid numbers increased, estimated both by HDE (Fig. 1) and by RRPE (Fig. 2). Thus, according to both models, A. gifuensis at all 4 tempera- (1.1323)TN N = (8) tures showed type II functional responses. Attack rates (a) and han- par 1+ (1.1323)(0.0129)N dling times (Th) of A. gifuensis were estimated by both HDE (Table 2) and RRPE (Table 3) at 4 temperatures. Equations 4, 5, 6, and 7 show the logistic regression analysis with estimated values of parameters at 15, (1.3142)TN Npar = (9) 20, 25, and 30 °C, respectively. 1+ (1.3142)(0.0105)N

N exp[4.759e + 00) + (–1.667e – 01)N + (2.143e – 03)N2 + (–9.754e – 06)N3] par = (4) N 1 + exp[4.759e + 00) + (–1.667e – 01)N + (2.143e – 03)N2 + (–9.754e – 06)N3] (1.3203)TN N = par 1+ (1.3203)(0.0120)N (10) N exp[1.099e + 01) + (–3.782e – 01)N + (4.667e – 03)N2 + (–1.968e – 05)N3] par = (5) N 1 + exp[1.099e + 01) + (–3.782e – 01)N + (4.667e – 03)N2 + (–1.968e – 05)N3] (1.7999)TN N = par 1+ (1.7999)(0.0214)N (11) N exp[5.244e + 00) + (–1.403e – 01)N + (1.428e – 03)N2 + (–5.524e – 06)N3] par = (6) N 1 + exp[5.244e + 00) + (–1.403e – 01)N + (1.428e – 03)N2 + (–5.524e – 06)N3]

Attack rates (a) and handling times (Th) of A. gifuensis modeled by N exp[2.176e + 00) + (–1.001e – 01)N + (1.263e – 03)N2 + (–5.664e – 06)N3] par = (7) RRPE are presented in Table 3. For 25 °C, R statistical software was un- N 1 + exp[2.176e + 00) + (–1.001e – 01)N + (1.263e – 03)N2 + (–5.664e – 06)N3] able to estimate parameter values, wherefore the attack rate (a) and

Table 1. Results of logistic regression analysis, with estimates and standard errors (SE) of linear, quadratic, and cubic coefficients for the proportion of aphids parasit- ized by Aphidius gifuensis against increasing aphid densities offered at various constant temperatures.

Temperature Coefficient Estimate SE Z value Pr(>| Z | )

15 °C Constant (P0) 4.759e+00 1.204e−01 39.51 <2e−16 ***

Linear (P1) −1.667e−01 6.506e−03 −25.63 <2e−16 ***

Quadratic (P2) 2.143e−03 1.094e−04 19.59 <2e−16 ***

Cubic (P3) −9.754e−06 5.753e−07 −16.96 <2e−16 ***

20 °C Constant (P0) 1.099e+01 2.981e−01 36.85 <2e−16 ***

Linear (P1) −3.782e−01 1.398e−02 −27.05 <2e−16 ***

Quadratic (P2) 4.667e−03 2.099e−04 22.23 <2e−16 ***

Cubic (P3) −1.968e−05 1.011e−06 −19.46 <2e−16 ***

25 °C Constant (P0) 5.244e+00 1.532e−01 34.22 <2e−16 ***

Linear (P1) −1.403e−01 7.930e−03 −17.7 <2e−16 ***

Quadratic (P2) 1.428e−03 1.292e−04 11.06 <2e−16 ***

Cubic (P3) −5.524e−06 6.631e−07 −8.33 <2e−16 ***

30 °C Constant (P0) 2.176e+00 7.392e−02 29.43 <2e−16 ***

Linear (P1) −1.001e−01 4.474e−03 −22.37 <2e−16 ***

Quadratic (P2) 1.263e−03 8.172e−05 15.46 <2e−16 ***

Cubic (P3) −5.664e−06 4.558e−07 −12.43 <2e−16 ***

Asterisks indicate significance level: ***, 0.001. Khan et al.: Functional response of Aphidius gifuensis on Myzus persicae 699

Fig. 1. Type II functional response curves fitted by Holling’s disc equation (HDE) ofAphidius gifuensis against Myzus persicae at various temperatures.

handling time (Th) were estimated by Solver tool in Microsoft Excel 2010. (4.295e + 03)T N = N 1 – exp – (14) This tool provides only the parameter values, so standard errors and oth- par   1 + (4.295e + 03)(0.0144)N  er statistical values at 25 °C could not be listed in Table 3. At 25 °C, the attack rate was 4.295e+03 −1d and was highest among all temperatures. At 20 °C, the attack rate was 1.153e+02 ± 3.655e+02 d−1 and was lower (1.4721)T N = N 1 – exp – (15) than at 25 °C. At 15 °C, the attack rate was 4.3759 ± 0.4184 −1d and was par   1 + (1.4721)(0.0218)N  lower than at 20 °C. At 30 °C, the attack rate was 1.4721 ± 0.1469 d−1 and was the lowest among all temperatures. As found with the HDE model, these results also showed that attack rates were highest at 20 and 25 °C. Discussion At 30 °C, the handling time was 0.0218 ± 0.0010 d and was the significantly longest among all the temperatures (Table 3). At 15 and 25 °C, handling times were the same with 0.0144 d and shorter than This study of functional responses was a preliminary step in evalu- at 30 °C. At 20 °C, the handling time was 1.265e−02 ± 3.808e−04 d and ating the efficiency of the parasitoid A. gifuensis in biological control was the shortest among all the temperatures. The handling time was programs (Overholt & Smith 1990). In our study, Petri dishes were not longest at 30 °C and shortest at 20 °C. Equations 12, 13, 14, and 15 used as in many previous studies (van Steenis & El-Khawass 1995; Don- show RRPE with modeled values of attack rate (a) and handling time nelly & Phillips 2001; Farrokhi et al. 2010). We believe that the use (T ) at 15, 20, 25, and 30 °C, respectively. of sweet peppers planted in pots provides a better understanding of h functional responses, because the environment is more open as com- (4.3759)T pared with Petri dishes. Our results demonstrated that temperature N = N 1 – exp – (12) par   1 + (4.3759)(0.0141)N  had a significant effect on the functional response A.of gifuensis to M.

persicae. At all 4 temperatures, linear parameters (P1) were negative (Table 1), showing that the functional responses were type II. A type (1.153e + 02)T N = N 1 – exp – (13) II functional response has been found by many scientists with other par   1 + (1.153e + 02)(1.265e – 02)N  insect species under various conditions (Bernal et al. 1994; De Clercq 700 2016 — Florida Entomologist — Volume 99, No. 4

Fig. 2. Type II functional response curves fitted by Roger’s random parasitoid equation (RRPE)Aphidius of gifuensis against Myzus persicae at various temperatures. et al. 2000; Zamani et al. 2006; Fathi & Nouri-Ganbalani 2009). Holling (Lepidoptera: Noctuidae). In the present study, at all temperatures A. (1959) stated that invertebrates display a type II functional response gifuensis showed a type II functional response. Functional response whereas type III is found in vertebrate predators, but later this idea types and estimated parameters for an insect species could be affected was rejected because parasitoids can also display a type III functional by many factors such as temperature, type of prey or host, and host response. Wang & Ferro (1998) found a type II functional response at plant (Juliano & Williams 1985; Coll & Ridgway 1995; Runjie et al. 1996; low temperatures and a type III functional response at high tempera- Messina & Hanks 1998; Moezipour et al. 2008). tures in experiments with Trichogramma ostriniae Pang & Chen (Hy- Our results also indicated that there was a considerable difference menoptera: Trichogrammatidae) parasitizing Ostrinia nubilalis Hübner between the values of parameters modeled by HDE and RRPE. Values

Table 2. Estimate and standard error (SE) of attack rate (a) and handling time (Th) of Aphidius gifuensis on Myzus persicae by Holling’s disc equation (HDE) at various constant temperatures.

Temperature Coefficient Estimate S.E. t value Pr(>| t | ) 15 °C Attack rate (a) (d−1) 1.1323 0.0191 59.21 <2e−16***

Handling time (Th) (d) 0.0129 0.0002 57.17 <2e−16*** 20 °C Attack rate (a) (d−1) 1.3142 0.0312 42.02 <2e−16***

Handling time (Th) (d) 0.0105 0.0002 38.50 <2e−16*** 25 °C Attack rate (a) (d−1) 1.3203 0.0415 31.78 <2e−16***

Handling time (Th) (d) 0.0120 0.0003 32.96 <2e−16*** 30 °C Attack rate (a) (d−1) 0.7999 0.0393 20.32 7.32e−14***

Handling time (Th) (d) 0.0214 0.0009 22.39 1.37e−14***

Asterisks indicate significance level: ***, 0.001. Khan et al.: Functional response of Aphidius gifuensis on Myzus persicae 701

Table 3. Estimate and standard error (SE) of attack rate (a) and handling time (Th) of Aphidius gifuensis on Myzus persicae by Roger’s random parasitoid equation (RRPE) at various constant temperatures.

Temperature Coefficient Estimate SE t value Pr(>| t | ) 15 °C Attack rate (a) (d−1) 4.3759 0.4184 10.46 4.47e−09

Handling time (Th) (d) 0.0141 0.0003 44.34 <2 −16*** 20 °C Attack rate (a) (d−1) 1.153e+02 3.655e+02 0.32 0.756

Handling time (Th) (d) 1.265e−02 3.808e−04 33.22 <2e−16*** 25 °C Attack rate (a) (d−1) 4.295e 03 N/A N/A N/A

Handling time (Th) (d) 0.0144 N/A N/A N/A 30 °C Attack rate (a) (d−1) 1.4721 0.1469 10.02 8.71e−09

Handling time (Th) (d) 0.0218 0.0010 20.99 4.16e−14

Asterisks indicate significance level: ***, 0.001; N/A denotes not available. of parameters modeled using RRPE were high, which might be due to 2013CB127600), and China Agriculture Research System (No.CARS- the exponential function (exp) in RRPE. For analysis of functional re- 25-B-06). We also thank anonymous reviewers for giving valuable sponse experiments, a good model is very important to understand- comments on the manuscript and all staff members of College of Plant ing the results. In this study, we tested 2 models. We compared HDE, Protection, Northwest Agriculture and Forestry University. which assumes constant host density and host replacement, with RRPE, which does not assume host replacement (Collins et al. 1981; Enkegaard 1994). HDE was better at estimating parameters compared References Cited with RRPM because the values of parameters modeled by HDE were simple, easy, and logical. Mohaghegh et al. (2001) and Allahyari et al. Allahyari H, Fard PA, Nozari J. 2004. Effects of host on functional response of offspring in two populations of Trissolcus grandis on the sunn pest. Journal (2004) also found that HDE was better at estimating parameters when of Applied Entomology 128: 39–43. compared with RRPE. Bernal JS, Bellows TS, González D. 1994. Functional response of Diaeretiella ra- Parasitism of A. gifuensis was higher between 20 and 25 °C and pae (McIntosh) (Hym., Aphidiidae) to Diuraphis noxia (Mordwilko) (Hom., lower at 15 and 30 °C, indicating that A. gifuensis performs best when Aphididae) hosts. Journal of Applied Entomology 118: 300–309. Berryman AA. 1999. The theoretical foundations of biological control, pp. 3–21 the temperature ranges from 20 to 25 °C. These results were similar In Hawkins BA, Cornell HV [eds.], Theoretical Approaches to Biological Con- to the findings of Ohta & Miura (2001). In our study, the highest at- trol. Cambridge University Press, Cambridge, United Kingdom. tack rate (a) modeled using HDE at 25 °C was 1.3203 ± 0.0415 d−1 and Coll M, Ridgway RL. 1995. Functional and numerical responses of Orius insid- modeled by RRPE was 4.295e+03 d−1. The difference in values might be iosus (Heteroptera: Anthocoridae) to its prey in different vegetable crops. due to the exponential function in RRPE. Gordon (1985) observed that Annals of the Entomological Society of America 88: 732–738. Collins M, Ward S, Dixon A. 1981. Handling time and the functional response of predation rate of Coleomegilla maculata (De Geer) (Coleoptera: Coc- Aphelinus thomsoni, a predator and parasite of the aphid Drepanosiphum cinellidae) on Leptinotarsa decemlineata (Say) (Coleoptera: Chrysome- platanoidis. Journal of Ecology 50: 479–487. lidae) eggs increased as temperature increased from 10 to 30 °C. Mack De Clercq P, Mohaghegh J, Tirry L. 2000. Effect of host plant on the functional & Smilowitz (1982a, b) observed that the predation rate ofC. maculata response of the predator Podisus nigrispinus (Heteroptera: Pentatomidae). Biological Control 18: 65–70. on M. persicae increased with temperature increase, but in our study Donnelly BE, Phillips TW. 2001. Functional response of Xylocoris flavipes (He- the attack rate (a) increased up to 25 °C and then decreased at 30 °C. miptera: Anthocoridae)—effects of prey species and habitat. Environmental At 30 °C, the attack rate (a) of A. gifuensis was very low. The lowest at- Entomology 30: 617–624. tack rate (a) modeled by HDE at 30 °C was 0.7999 ± 0.0393 d−1 and by Enkegaard A. 1994. Temperature dependent functional response of Encarsia RRPE was 1.4721 ± 0.1469 d−1, indicating that the performance of the formosa parasitizing the Poinsettia-strain of the cotton whitefly Bemisia tabaci on Poinsettia. Entomologia Experimentalis et Applicata 73: 19–29. parasitoid is adversely affected by high temperatures. Handling times Farrokhi S, Ashouri A, Shirazi J, Allahvari H, Huigens ME. 2010. A comparative

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